The emotional states and associated behavioral responses (flexible‐adaptive behaviors vs. inflexible‐maladaptive behaviors) of cancer patients during the SARS‐CoV‐2 outbreak: A multi‐center cross‐sectional study in Italy

Abstract Objective Distress during SARS‐CoV‐2 outbreak affected also cancer patients' well‐being. Aim of this study was to investigate patient' reactions and behavior (flexible‐adaptive vs. inflexible‐maladaptive) during the SARS‐CoV‐2 outbreak. Methods A cross‐sectional survey was designed with a self‐report questionnaire, “the ImpACT questionnaire,” developed for the study. Regression analysis was performed on data. Results Four hundred and forty five cancer patients from 17 Italian regions participated in the study. 79.8% of participants were female (mean age of 58 years). 92.6% of participants reported feeling vulnerable to COVID‐19 contagion; 75.6% reported helpless, 62.7% sad, 60.4% anxious, and 52.0% anger. Avoidance of thinking about coronavirus is the principal maladaptive behavior that emerged. Participants who reported feeling anxious were more likely to have fear of staff being infected with COVID‐19 (OR = 3.01; 95% CI = 1.49–6.30) and to have disrupted sleep due to worry (OR = 2.42; 95% CI = 1.23–4.83). Younger participants reported more anxiety (OR = 0.97; 95% CI = 0.94–1.00); men reported feeling calm more than women (OR = 2.60; 95% CI = 1.27–5.43). Conclusions Majority of cancer patients reported serious concerns regarding SARS‐CoV‐2 infection; reliable information and psychological support must be offers to respond to these needs.


| BACKGROUND
A considerable amount of evidence has shown the correlation between the SARS-CoV-2 outbreak and the increased risk of cancer patients suffering adverse psychological effects, [1][2][3][4] including worsening of anxiety, 5 distress, [6][7][8] depression, 9 loss of energy, and quality of life. 10,11verexposure to SARS-CoV-2 related information has also increased distress and the inability to disengage from information flow. 6,12s SARS-CoV-2 has become a major stressor, several studies reported increased stress levels in nurses, physicians, and radiographers. 13,14The organizational characteristics of the workplace, along with the social appreciation of the job position, significantly influence overall satisfaction with life. 15onetheless, cancer patients generally have been of good opinion regarding the medical attention they received during the pandemic, and satisfaction with received care is a good predictor of emotional patients wellbeing. 3,6ther studies have focused on specific aspects of psychological health during the SARS-CoV-2 outbreak, seeking to identify which aspects might best explain protective and destructive emotional responses in patients. 3,16,17Specifically, several studies have shown that dispositional psychological flexibility is key in ensuring good psychological health. 18sychological flexibility has been shown to be highly conducive in the establishment and maintenance of mental wellbeing 19,20 and enables individuals to adapt to changing circumstances by altering their behavior without compromising their personal values. 18Psychological flexibility is defined as "one's intentions to display situation-appropriate behaviors" 21 and has been shown to be a robust predictor of effective problem-focused and emotion-focused coping strategies during stressful events. 22sychological flexibility is a core component of ACT and may be crucial in understanding how individuals are affected by, and cope with, the significant challenges brought on by cancer and its treatments.Psychological flexibility is defined as the ability to identify and adapt to situational demands in an attempt to improve longerterm outcomes in a way that is personally meaningful.It has been associated with improved psychological health, quality of life, and well-being in both clinical and nonclinical populations including both distress-related and positive outcomes (e.g., benefit finding) in cancer survivors.Furthermore, psychological flexibility has been shown to be amenable to change over time, presenting a potential target for interventions. 23,24n contrast, psychologically inflexible behaviors, which are dysfunctional and contextually non-adaptive, manifests as rigid psychological reactions. 25For instance, inflexible behaviors can include the radical avoidance of interpersonal relationships, the excessive consumption of food, or an increased use of alcohol and/or cigarettes. 3In such a context, people can feel overwhelmed by uncontrollable fear.In contrast, embracing (rather than avoiding) inner discomfort and accepting unwanted thoughts, while also engaging in values-based action, increases resilience during adversity. 26,27ur study aimed to investigate the emotional states and associated behavioral responses (flexible-adaptive behaviors vs. inflexible-maladaptive behaviors) of cancer patients during the SARS-CoV-2 outbreak in Italy.

| Procedure
We have developed a cross-sectional study with a snowball sampling strategy that focused on recruiting oncological patients from Italian oncology operating units was utilized.
Italian patients over 18 years of age with oncological conditions, not affected by COVID-19, were eligible to participate in the study.
Potential respondents were invited to complete an anonymous survey, and, after informed consent was obtained, a digital or paper version (depending on access to the hospital for medical visits) of the questionnaire was administered.
Ethics approval was obtained from the Ethical Committee for Clinical Trials of the Provinces of Verona and Rovigo in Northern Italy (Prog.2642 CESC), which conformed to the principles embodied in the Declaration of Helsinki.
Data collection took place over 1 month after the WHO had declared the SARS-CoV-2 outbreak (April 2020-May 2020).The data that support the findings of this study are available from the corresponding author upon reasonable request.

| Outcome variable
In order to evaluate emotional states and their associated behavior, we developed a 31-item "ImpACT" self-report questionnaire.The result of self-rated emotional states was the primary outcome variable for the study.Three different emotional states, occurring during the pandemic (April 2020-May 2020), were assessed by asking participants whether or not they agreed with the following statements: "I feel anxious," "I feel angry," and "I feel calm." In the first part of the questionnaire, study participants were asked to respond to the question, "How do you feel about the coronavirus right now?" by reporting their emotional state (calm, indifferent, sad, feeling at fault towards family members, feeling powerless, angry, nervous or restless, worried, anxious, scared, or panicked) as compared to that of prior to the SARS-CoV-2 outbreak.

| Primary explanatory variable
Participant behavior was the primary explanatory variable for the study.The second part of the questionnaire was developed in order to elaborate on the behaviors associated with the emotional states identified in part one.The "ImpACT" questionnaire has been used previously for patients with various conditions. 3It was specifically adapted for cancer patients by changing the words "doctor" to "oncologist" and "medical center" to "oncological center." Respondents used a 5-point Likert scale, ranging from 0 "never true" to 5 "always true", to rate different behaviors with respect to both the internal context (thoughts, emotions, and physical sensations) and the external context (external stimuli, including the context of care).
Consistent with the ACT model (based on functional contextualistic science), 19,20 two types of behaviors were investigated: (1) adaptive and flexible behaviors (e.g., openness to emotional experience and the acceptance of aversive emotions, thoughts, or physical sensations); and (2) inflexible/maladaptive behaviors (e.g., experiential avoidance function, including the avoidance or suppression of unwanted emotions with alcohol or other substances or by using distraction techniques) in an attempt to control and redirect internal experience.

| Effect modifiers variables
The sociodemographic variables potentially influencing medical and psychological aspects were controlled for in a multivariable analysis.This allowed us to isolate the effects of sociodemographic, medical, and psychological factors that may affect the self-rating of emotional states.
Sociodemographic variables included gender, age, education history, residential location, marital status, employment status, economic losses related to the SARS-CoV-2 outbreak, parental status, family network, household size and layout (number of rooms, garden, balcony, etc.), cohabitation status before and during quarantine, and social isolation regulations.Respondents were also asked for information regarding their life context, including their principal sources of information regarding SARS-CoV-2 and COVID-19 symptom management.Participants were also asked about their trust in said sources and any role the information may have played in providing psychological support.
Medical variables included the participants' specific pathology, physical health status, medical history, and treatment phase (diagnostic, active therapy, follow-up, palliative care).
Psychological variables included psychological health status, psychiatric/psychological history, emotional status as related to SARS-CoV-2 and COVID-19, behaviors in response to the fear of developing COVID-19 (including avoidance behaviors and the use of substances such as alcohol).

| Statistical analysis
Summary statistics were calculated for all variables.The 31 items of the ImpACT questionnaire were condensed from a 5-point Likert scale into a binary response ("Never true," "Rarely to always true").Items 5, 17, and 31 were excluded from further analyses due to a lack of variation in the responses given.Participant sex, age, and the ImpACT questionnaire item responses were analyzed using univariable logistic regression models to explore their association with three different dependent variables describing patients' emotional states during the pandemic: anxiety, anger, and calmness.Emotions were assessed via agreement (yes or no) with the statement: "I feel anxious," "I feel angry," and "I feel calm."Only variables signifiantly associated (p-value < 0.2) with the three different emotional states were included in the full logistic regression model.The Akaike Information Criterion (AIC) was used to compare candidate models.Goodnessof-fit measures were estimated for these models.All pvalues were two-tailed, with a significance level of 0.05.Analyses were performed using R software, version 3.6.1.

| Participants
The sample consisted of 445 cancer patients from across 17 Italian regions, with most participants coming from three regions of northern Italy (Veneto, Lombardy, Piedmont).The sociodemographic characteristics of participants are shown in Table 1.79.8% of participants were female, while the mean age was 58 years.66.3% of participants held a high school certificate or higher education degree.69.9% were married or in a relationship, and 76.6% reported having children, of which 49.2% had more than two.The year of cancer diagnosis ranged from 1987 to 2020, and 25.3% of participants reported having had a relapse.The most common oncological diagnosis was found to be breast cancer (36.2%).59.6% of patients reported being in the active 12 [5-20]   Abbreviations: IQR, interquartile range; NET, neuro endocrine tumors.a Patients may report more than one treatment; therefore, percentages do not sum to 100%.
phase of treatment, and 33.18% in the follow-up phase.
The most commonly reported cancer therapy was chemotherapy (55.1%).24.2% of participants reported having had a psychological problem before the SARS-CoV-2 outbreak, with anxiety and depression being the most common disorders (9.7% and 6.7% of cases, respectively).Most participants (75.1%) reported that they considered the Ministry of Health, Civil Protection and Italian National Institute of Health to be trusted sources of information.Newspapers and television were trusted by around half of participants (54.6%), whereas medical professionals such as oncologists (27.2%), physicians (21.3%), and nurses (11.2%) were trusted by fewer participants.Mass media (17.1%), relatives (13.9%), psychologists (4.9%), social media (3.6%), and radio broadcasts (0.2%) were trusted to varying degrees.
Most participants reported being satisfied with the information received from oncologists (85.9%), nurses (81.0%), and psychologists (72.1%), whereas the responses given by physicians (66.3%) and emergency room staff (58.3%) proved to be appreciated by a lower proportion of participants.Further to this, although 87.0% of individuals reported keeping themselves informed about SARS-CoV-2 and to feel confused about the information they had received.Most patients (97.6%) reported strictly adhering to the physical distancing and PPE regulations that were stipulated by the government and medical professionals.Just over half of participants (59.8%) reported feeling safe in their oncology unit.56.5% feared to some degree that medical staff would fall ill with COVID-19, and 51.3% said they were afraid of disruption to ongoing medical care.33.9% of participants reported having contacted their oncologist more frequently than so in the past, and 12.8% reported having canceled appointments with the oncologist.Most participants (74.5%) reported that the relationship with their partner and their openness towards their relatives had not changed by that stage of the pandemic, and 58.1% declared to have remained in contact with other cancer sufferers.21.6% of participants said they did not leave home for fear of being exposed to SARS-CoV-2.36.3% of participants preferred to not leave the house, and 38.0% avoided all contact with others.Most participants (87.7%) reported significant changes to their lives as compared to before the SARS-CoV-2 outbreak.56.2% reported feeling more alone than in the past, and 34.5% reported being unsatisfied with life.

| Regression analysis
In the multivariable model, after controlling for potential confounders, three different clusters of emotional states were considered (a) feeling calm, (b) feeling anxious, and (c) feeling angry, and their association with the items of the ImpACT questionnaire and sociodemographic variables were investigated. 3.2.1 | Cluster of participants who feel "calm" About half of participants (45.5%) reported feeling calm during the investigated period of the COVID-19 pandemic, with most participants reporting not feeling indifferent to the situation (93.5%).
Furthermore, 52.0% of participants reported experiencing anger, and 7.8% reported anger towards those who break the rules.

| DISCUSSION
Our results suggest that many cancer patients have faced the SARS-CoV-2 outbreak with a high degree of concern for their own health and for that of their loved ones.
Most study participants reported changes in their lives since the SARS-CoV-2 outbreak began, with many feeling more alone than in the past.Further to this, about a third of those surveyed reported being unsatisfied in life.
Unlike other published studies, in which participants reported an excess of SARS-CoV-2 information, 6,12 it seems that Italian cancer patients were generally satisfied with the information they obtained from their oncologists.
Indeed, most participants reported feeling well informed about SARS-CoV-2 by the oncologist and very safe in their cancer care center.
Consistent with other findings, in which it emerged that during lockdown, 35.2% of patients had canceled an Abbreviation: CI, confidence interval.
appointment with their specialist doctor due to their fear of becoming infected with SARS-CoV-2 and that 29.4% had done so after lockdown. 3About one in 10 of the cancer patients surveyed here had canceled appointments with their oncologists.Further to this, about a third had contacted their doctor more so than in the past.
For each of the emotional states investigated in our study, the associated behavioral reactions (adaptive and flexible behaviors vs. maladaptive and inflexible behaviors) were analyzed.
Almost all of the sample reported paying close attention to possible COVID-19 symptoms.This concern was managed in different ways, ranging from feeling aware of the situation but calm (for almost half of the sample) to emotional states characterized by worry, nervousness, anxiety, helplessness, feelings of guilt, sadness, and/or anger (with anger being directed towards those breaking lockdown rules especially).Such changes in emotional state would manifest as disrupted sleeping patterns; however, no evidence was apparent of increased alcohol use, food intake, or smoking among participants as means of avoiding unpleasant emotions.
Male participants reported feeling calmer than women, being less fearful of the future, and suffering less insomnia due to worry.
Participants who reported feeling anxious had more concerns about the health of medical staff, experienced more sleep disruption due to worry, had a greater reliance on their faith, and a greater propensity to use psychotropic medications to manage anxiety.
Participants who reported feeling anger during the SARS-CoV-2 outbreak showed a greater tendency to try and avoid thinking about coronavirus.
In line with a previous study, 3 some behaviors arguably served an experiential avoidance function (e.g., asking for reassurance may reflect an attempt to avoid or control fear (item 10), and increasing food intake or alcohol use be done so in an effort to avoid negative emotions (item 22)).Experiential avoidance appears to be a highly dysfunctional strategy in contexts such as pandemics and is an important vulnerability factor for poor psychological health 17,[25][26][27][28] that correlates with increased anxiety, distress, depression, 3 and insomnia. 29,30urthermore, angrier participants were at greater risk of feeling lonely and reported avoiding thinking about coronavirus more often.Generally speaking, such thought suppression tends to have a paradoxical effect and actually increases rumination of thoughts, resulting in increased discomfort, anxiety, frustration and anger.
Importantly, studies have shown that feelings of loneliness often precipitate psychological problems.Preexisting depression was identified in 12% of participants, while another study has demonstrated that individuals experiencing loneliness during the pandemic were 4.5 times at higher risk of depression. 31This correlates with other research suggesting that loneliness is an unintended consequence of COVID-19 restrictions and that it aggravates pre-existing depression. 32inally, one in five of the cancer patients that participated in our study sought support from a psychologist to help manage their fears and alleviate emotional suffering.

| Strengths and limitations
The main difficulty in this study has been distinguishing between emotional states due to the SARS-CoV-2 outbreak and those potentially arising as a consequence of oncological pathology.The questionnaire was carefully designed with this in mind.Subjects were contacted and recruited directly by the researchers, who collected the data primarily using paper questionnaires.As a direct approach, this may have encouraged the participation of a greater number of individuals than an open advertisement requesting participants would have done; however, the "snowball sampling strategy," as a recruiting method, may have created a possible selection bias.Furthermore, data cannot be generalized due to the nature of a questionnaire built ad hoc to analyze cancer patients' perspectives in this particular situation.

| Clinical implications
Assessing cancer patient's behavior and reaction during a huge stressful event such as COVID-19 outbreak could Abbreviation: CI, confidence interval.
be extremely important from a clinical point of view.If not recognized and treated adequately, these psychological effects could have strong impacts on cancer patients' psychophysical health, quality of life, and social dynamics (both at home and at work).This could potentially translate into an increased burden on the national healthcare system.Therefore, the way in which healthcare professionals recognize and respond to patients' needs, facilitate understanding of information, and how they offer appropriate and timely emotional support is ever more relevant.

| CONCLUSIONS
These results suggest that the majority of cancer patients participating in our study had concerns about developing COVID-19 and about their health in general.Furthermore, feelings of uncertainty regarding the management and implementation of their cancer treatment have also been identified.Cancer often presents as a life-threatening condition, and understandably patients are anxious about their diagnosis, treatment, prognosis, and disease stage.The SARS-CoV-2 outbreak has exacerbated many of these fears, which, along with concerns about developing COVID-19, has resulted in an increased feeling of insecurity, fragility, and loneliness.Patients mainly reported feelings of anxiety and anger and engaging in non-functional and, at times, risky behaviors in efforts to manage their distress.
Participants demographics and clinical characteristics of overall sample.
T A B L E 1 Multivariate logistic regressions.Dependent variables identify participants who report feeling anxious.Multivariate logistic regressions.Dependent variables identify participants who reported feeling calm.
T A B L E 3 T A B L E 2Note: Dependent variables identify participants who reported feeling calm.
Multivariate logistic regressions.Dependent variables identify participants who reported feeling angry.
T A B L E 4Note: Dependent variables identify participants who reported feeling angry.